Download Electron Transfer in Chemistry and Biology – The Primary Events in

Primary Events in Photosynthesis
Electron Transfer in Chemistry and Biology –
The Primary Events in Photosynthesis
V Krishnan
One of the most important chemical reactions is electron
transfer from one atomic/molecular unit to another. This
reaction, accompanied by proton and hydrogen atom transfers, occurs in a cascade in many biological processes, including photosynthesis. The key chemical steps involved in photosynthesis and the many unsolved mysteries are described in
this article.
V Krishnan is Professor at
the Department of
Introduction
Inorganic and Physical
Chemistry, Indian Institute
In the centenary year of the discovery of the electron by J J Thomson
it would be most appropriate to recount how such a discovery has
really enlarged our understanding of many facets of chemistry and
biology. Chemistry as it is practised today cannot exist without a
proper appreciation of the role of the electron. The concept of a
chemical bond as the electron distribution holding atoms together
has revolutionised our knowledge about molecules, their structures
and stabilities. Our understanding of chemical reactions has also
undergone a fundamental change after the discovery of the electron.
In gross terms, chemical reactions appear to be addition, removal
and rearrangement of atoms. At a deeper level, chemical transformations always involve electrons shifting from one atom or molecule to
another thereby creating new molecules.
Consider the well-known reactions – oxidation and reduction. They
essentially involve oxygen and hydrogen. Oxidation means ‘addition of oxygen’ and reduction implies ‘removal of oxygen’. One can
replace this statement by loss or acquisition of hydrogen atoms. With
the electrons coming into the scene, oxidation and reduction can be
defined as processes which lead to loss and gain of electrons,
respectively. This has entirely changed the earlier framework of
interpreting reactions in chemistry and biology. This shift in
RESONANCE  December 2011
of Science, Bangalore. His
major research interests
lie in the model reactions
of photosynthetic process
with a view to obtaining
synthetic leaf. He is also
an Honorary Professor
and Head, Academic
Programmes of the
Jawaharlal Nehru Centre
for Advanced Scientific
Research, Jakkur,
Bangalore.
Keywords
Photo-induced electron transfer,
photosynthesis, charge transfer
reactions, electron transfer proteins, donor–acceptor process.
Appeared in Vol.2, No.12, pp.77–86,1997.
1201
V Krishnan
emphasis enables one to understand the elementary steps of complex chemical reactions.
In this article, the electron transfer (ET) process is described.
Chemical systems in which ET is likely to be facile are first discussed. The important role of ET in many biological processes is
then pointed out, with special reference to photosynthesis. Many
unusual features in the reaction sequence and current attempts to
resolve a few questions are also highlighted.
Electron Transfer in Ground and Excited States
Photo-induced
electron transfer
(PET) is a very
important process,
with considerable
chemical and
biological
relevance.
Electrons are not bound equally strongly in all atoms and molecules.
Some have greater affinity for the electron than others. Electron rich
systems which can readily give up an electron are called Donors (D).
Correspondingly, electron deficient units which have the ability to
pick up an electron are referred to as Acceptors (A). A few examples
of molecules which can function as electron donors and acceptors
are shown in Box 1.
When systems with varying capacity to hold the electron are brought
together, there is a likelihood of an electron hopping from the
weakly bound to the strongly bound unit. Thus, electron transfer is
possible when D and A type molecules are allowed to interact. There
is another mode by which electron transfer can take place. By
absorption of light of suitable wavelength, molecules (especially
those containing chromophoric groups) can be induced to undergo
transition from the ground to the excited electronic state. Molecules
in the excited electronic state are generally very reactive. They are
capable of giving up (or taking in) an electron if efficient acceptor or
donor units are available in the neighbourhood. Such photo-induced
electron transfer (PET) is a very important process, with considerable chemical and biological relevance.
There are many features of the ET process which are of fundamental interest. First, we need quantitative criteria for identifying
donors and acceptors. Methods are required to prove the occurrence
1202
RESONANCE  December 2011
Primary Events in Photosynthesis
Box 1. A few Examples of Donor/Acceptor Molecules
DONOR
RESONANCE  December 2011
ACCEPTOR
1203
V Krishnan
Electron transfer
reactions can be
studied using
spectroscopic
methods which
probe the
energetic and spin
states of electrons
in molecules.
of electron transfer. The rate of the reaction is, of course, of prime
importance. Therefore, techniques which allow measurement of
rates of very fast reactions are needed. Finally, a reliable theoretical
framework is necessary for interpreting the contributions of various
factors which determine the efficiency of electron transfer. In the
last few decades, intense research has gone on along these lines.
How well a molecule can function as a donor is related to the ease
with which an electron can be taken away from the molecule.
Therefore, the ionization energy of the molecule (ID), which is the
minimum energy required to remove an electron from a molecule in
its ground state, is an excellent criterion. This quantity can be
obtained from photoelectron spectroscopy measurements. In a similar fashion, one can define an acceptor. A good acceptor is one with
a higher electron affinity value (EA), i.e., the energy gained by a
molecule on accepting an electron and retaining it within itself. If
one knows the ID and EA values, one can classify all the molecules
in terms of donors and acceptors. Equivalently, donor and acceptor
abilities can be quantified in terms of oxidation and reduction
potentials.
Armed with the knowledge of donor and acceptor molecules, one
can ascertain in a reaction whether the electron really has left the
donor molecule or not (alternatively, whether an acceptor molecule
has really received the electron from the donor or not). Many
different experimental techniques can be used to probe the electron
transfer reaction. In certain cases, electron spin resonance would be
helpful. It is often easier to monitor the nature of the donor molecule
after it has performed its donor function (which means it becomes
positively charged) and the negatively charged acceptor subsequent
to the receipt of the electron through other spectroscopic methods.
New electronic absorption or emission bands may appear. Intensity
changes may also provide information about the nature of the
species.
The next question is how fast the electron moved from the donor to
the acceptor in a reaction. This is an important aspect in chemistry
which has great relevance in biological reactions such as certain
1204
RESONANCE  December 2011
Primary Events in Photosynthesis
enzyme functions, photosynthesis and others. The study of fast rate
processes has become possible with the advent of lasers. Spectral
signatures can be monitored in very short time scales. Reactions
occurring in nano (10–9), pico (10–12) and even femto (10–15) seconds
can now be studied.
The importance of electron transfer lies in the fact that it is often
immediately followed by several further reactions. Hydrogen atom
and proton transfers are especially facilitated by an initial electron
transfer. If the role of the electron is not recognized, the subsequent
deep-seated chemical changes would appear to be driven by a
mysterious force.
Proteins containing
metal ions which
can adopt different
oxidation states
facilitate electron
transfer.
Electron Transfer in Biology
Electron transfer reactions are fast, can occur across relatively well
separated units, can be triggered by light and can induce secondary
reactions. All these features are fully exploited by nature. Biological
processes involve complex reactions dominated by electron and
hydrogen movement. There are proteins that facilitate electron
transfer from one part to another. A few such systems are listed in
Box 2.
These proteins have metal ions capable of existing in different
oxidation states. The ions are embedded in an environment (ligand
Box 2. A few examples of Electron Transfer Proteins
Protein
Cytochromes
Metal ions
Fe
a, a3, b, c1, c, etc.
cyt. aa3
Ferridoxins
Fe
Rubredoxins
Fe
Xanthine oxidase
Fe/Mo
Aldehyde oxidase
Fe/Mo
Succinate dehydrogenase
Stellacyanin, plastocyanin and
azurin
RESONANCE  December 2011
Cu
1205
V Krishnan
Figure 1. Molecular structure of the plant pigments,
tetrapyrrole units. (a) Chlorophyll a, (Chl),
(b)
Bacterio
Chlorophyll
(B.Chl) and (c) a model
compound, tetraphenyl
porphyrin.
system) that responds to change in the oxidation states to transfer an
electron from one part to another. The important ligand systems are
tetrapyrrole macrocycles, viz., porphyrins (Figure 1). Subsequent
to the movement of electrons through these arrays of molecules, the
electrons are finally captured by biological acceptor molecules.
Throughout this electron transfer, there is a corresponding movement of protons elsewhere in the vicinity of the system to maintain
the electrical neutrality so as to avoid accumulation of charges.
The electron transfers are manifested in the catalytic conversion
processes (enzyme functions) of these substrates. A few such
reactions are: (i) conversion of chemically inert molecular nitrogen
to the reduced products, (ii) conversion of peroxides to molecular
oxygen, and (iii) substitution of oxygen to the organic substrates
resulting in hydroxylated and other products. In all these events,
electrons are transferred from the enzyme to the substrate with
subsequent abstraction of hydrogen from the neighbouring molecules. Prior to the discovery of electrons, it was thought that such
reactions occur through some ‘reactive intermediates’ (catalytic
routes) involving hydrogens. The electron transfers between molecules in these systems have qualitatively improved our understanding.
Photosynthesis
Plants have been in existence for a long time even before humans.
1206
RESONANCE  December 2011
Primary Events in Photosynthesis
How do they support themselves and at the same time provide food
for other beings? It is through photosynthesis, one of the most
fascinating reactions in biology. It is this reaction which sustains life
on earth (Figure 2). This process provides energy to drive all life’s
activities such as chemical synthesis, mechanical work, osmotic
work, electric signals and others.
In chemical terms, photosynthesis can be represented by a simple
equation.
green
6 CO2 + 6 H2O + light —————> 6 O2 + (CH2O)6 + 112 Kcal/mol
plants
Certain bacterial systems do perform photosynthesis, i.e., synthesise
organic matter with the help of light. But instead of H2O they use
other compounds. In terms of oxidation – reduction, photosynthesis
can be thought of as removal of oxygen from CO2 and removal of
hydrogen from water. Alternately, the reaction involves transfer of
hydrogen atoms from water to CO2. This was the status of under-
Figure 2. Representation
of the various reactions of
photosynthesis.
RESONANCE  December 2011
1207
V Krishnan
Figure 3. Thylakoid membrane model showing the
possible location of various proteins, light harvesting (LH), reaction centre
(RC) and other pigments.
standing prior to the discovery of electrons. The classification of
molecules into donors and acceptors of electrons, the possibility of
excited donors and the many experimental methods (laser spectroscopy, photoncounting, ‘hole’ burning and others) have considerably
enhanced our understanding of this complex process.
Figure 4. The symmetric
arrangement of pigments
in the Photosynthetic
Reaction Centre of the
Bacterium Rhodobacter
Sphaeroides. The protein
part is not shown. The sequence of pigments : B.Chl
- special pair, on the top,
followed by B. Chl., B.
Pheophytin (pigment without the Mg atom) and
quinone in the bottom of
the figure.
1208
The photosynthesis process essentially occurs in a membrane composed of two components, light harvesting proteins (LHP) and
reaction centre proteins (RC) (Figure 3). The primary actions are
the harvesting of the light energy from the sun by a large number of
chlorophyll molecules and the efficient transduction of energy to an
RC complex wherein the electrons are released. The molecular
architecture of an RC complex in a membrane bound protein
(Figure 4) was determined by H Michel, J Deisenhofer and R Huber
using X-ray diffraction. This afforded the detailed electron transfer
pathways that led to a better understanding of the primary event.
RESONANCE  December 2011
Primary Events in Photosynthesis
It is found that the light energy is initially received by a ‘special pair’
bacteriochlorophyll molecule. The primary donor undergoes a rapid
charge separation and the electron rapidly cascades through one of
the arms to reach an electron acceptor molecule located at the
bottom. The charge separation event essentially occurs on photoirradiation. The sequence of molecules through which the electron
from the primary donor passes has been experimentally found and
the scheme is given below. The most important aspect of these
reactions is that the rate of electron transfer events is independent of
temperature in contrast to all the other chemical reactions. Hence
primary photosynthetic reactions occur at a relatively low temperature without any change in the efficiency.
There have been a few intriguing aspects in the process that have
caught the imagination of chemists. Why does an electron from the
primary donor bypass a chlorophyll molecule in the immediate
neighbourhood and pass off to a pheophytin molecule and then to
the quinones? Why don’t the electrons directly reach the quinone?
Interestingly, the electron transfer occurs only through one arm of
the entire complex with the molecules on the other arm remaining
mute witnesses to the electron passing through. The exceptionally
short time scales involved in the ET processes and also their variations are further challenging questions.
h
Ant -Ant-D-A-Q ————>1Ant*-Ant-D-A-Q
EET
EET
1
*
—————> Ant - Ant -D-A-Q ———> Ant -Ant-1D*-A-Q
c.a 0.01 ps
c.a.0.1ps
ET
————> Ant-Ant-D± A-Q ———> Ant-Ant-D+-A --Q
0.025 ps
ET
————> Ant-Ant-D+-A-Q-
2-4 ps
EET = Excitation energy transfer
ET = Electron transfer
Ant = antenna protein (LH)
D = primary donor
Bchl = special pair
A = B. Pheophytin
200 ps
Q = quinone
( See Figures 3 and 4)
1ps = 10-12 s.
RESONANCE  December 2011
1209
V Krishnan
Suggested Reading
E Rabinowitch

and G
Govindjee.Photosynthesis.
John Wiley and Sons. Inc.
New York, 1969.
G

Govindjee and R
Govindjee. Sci. Am. Dec.
pp. 132, 1974.
J Deisenhofer, O Epp, K

Miki, R Huber and H
Michel, Nature, 318, 618
(1985).
In order to derive possible answers, chemists construct and study
model molecular systems to duplicate the primary event of photosynthesis. For example, a number of molecules have been synthesized in which donor and acceptor units are placed at prefixed
distances and orientations. The rates of electron transfer have been
determined. These studies have shown that electron transfer rates
between an independent donor and acceptor or covalently linked
donor–acceptor combinations depend on many factors such as distal
separation between D and A, relative orientation of D with respect
to A, the nature of the medium and the nature of the covalent linkage
between the D and A.
R W Hary.Bioinorganic

Chem istry. Ellis Harwood. Chichester. New
York, 1984.
M A Fox and M Channon

eds.. Photo-induced electron transfer. Elsevier.
Amsterdam, 1988.
J Deisenhofer and H

Michel.
Angewandte
Chemie. Int. Edn. Engl.
28.829, 1989.
R Huber. Angewandte

Chemie.28.848, 1989.
Among the many model reactions, the simplest one is a donor
chemically linked to a series of acceptors and terminating in a
quinone. The chemical attachment is essential to put the acceptors in
a sequence depending on their electron affinities. The results of
these sustained efforts on model reactions have pointed out that
there is a requirement of a critical distance of 5 to 8 Å between the
donor and acceptor for maximum ket value and proper orientation of
D and A molecules so as to have their donor/acceptor orbitals in the
right orientation. The solvent medium also plays a very important
role in the rate of electron transfers.
The model reactions to mimic primary events have thus far succeeded in matching the rates in electron transfer reactions. However,
they have been unable to reproduce the temperature effect. Much
more work remains to be done on the natural systems and synthetic
models of photosynthesis before we can claim to have understood
the role of the electron in this fascinating biological process in its
entirety.
Address for Correspondence
V Krishnan
Department of Inorganic and
Physical Chemistry
Indian Institute of Science
Bangalore 560 012, India.
email:
[email protected]
1210
RESONANCE  December 2011